Brissopsis lyrifera and Amphiura chiajei in circalittoral mud

SS.SMu.CFiMu.BlyrAchi

SS.SMu.CFiMu.BlyrAchi recorded () and expected () distribution in Britain and Ireland (see below)

Ecological and functional relationships

The presence of the characterizing and other species in this biotope is primarily determined by the occurrence of a suitable substratum rather than by interspecific interactions. Brissopsis lyrifera and Amphiura chiajei are functionally dissimilar and are not necessarily associated with each other but for their occurrence in the same muddy sediments. Hollertz et al. (1998) found evidence of indirect competition between Brissopsis lyrifera and Amphiura chiajei. Decreased body and gonad growth rates in Amphiura chiajei were reported in the presence of Brissopsis lyrifera, possibly indicating that Brissopsis lyrifera may be a superior competitor for food, or that the deeper burrowing activity of Brissopsis lyrifera disturbs Amphiura chiajei

Bioturbation is particularly important in controlling chemical, physical and biological processes in marine sediments, especially when the influences of physical disturbances such as wave action or strong currents are minimized (Widdicombe & Austen, 1999). Hollertz (1998) estimated the turnover rate of sediment by Brissopsis lyrifera to be 8.0 cm² per hour, thus it is likely that Brissopsis lyrifera plays an important role in the enhancement of species heterogeneity in an otherwise largely homogenous environment.Brissopsis lyrifera is reported to increase meiobenthic species abundance and diversity and have a density dependent effect upon the community structure of meiobenthic nematode communities (Widdicombe & Austen, 1998; Austen & Widdicombe, 1998). The presence of Brissopsis lyrifera also significantly influenced nutrient fluxes of nitrogen and phosphorus at the sediment-water interface, owing to its burrowing activity promoting oxygenation of the substrata. Also with a high density of Brissopsis lyrifera (71 individuals per m²), silicate precipitation from the water column was observed to increase, probably owing to continuous bioturbation exposing a greater volume of sediment to the light, enabling autotrophs such as diatoms and radiolarians, to exist deeper in the substrata rather than as a thin surface film, increasing the biological demand for dissolved silicates (Widdicombe & Austen,1998)

The burrowing and feeding activities of Brissopsis lyrifera and Amphiura chiajei and other macrofauna, are likely to modify the fabric and increase the mean particle size of the upper layers of the substrata by aggregation of fine particles into faecal pellets. Such actions create a more open sediment fabric with a higher water content which affects the rigidity of the seabed (Rowden et al., 1998). Such alteration of the substratum surface can affect rates of particle resuspension.

Most of the species living in deep mud biotopes are generally cryptic so are protected to some extent from visual surface predators. However, the arm tips of Amphiura chiajei are an important food source for demersal fish and Nephrops norvegicus providing significant energy transfer to higher trophic levels. Munday (1993) examined the occurrence and significance of arm regeneration in Amphiura chiajei in a population from western Ireland. Biomass assays revealed that regenerative tissue accounted for up to 57.9% of total body weight with an overall mean of 4.21±0.3 arms per individual regenerating. Increased nutrients leading to increased primary production may contribute to an accumulation of hydrophobic contaminants in Amphiura chiajei and their transfer to higher trophic levels (Gunnarsson & Skold, 1999).

Nephrops norvegicus is eaten by a variety of bottom-feeding fish, including cod, haddock, skate and lesser spotted catshark (dog fish). There are also numerous records of fish predation on thalassinidean mud shrimps such as Calocaris macandreae which has been found in the stomachs of cod and haddock. Nephrops norvegicus is carnivorous, feeding on brittle stars, polychaetes and other crustaceans such as Calocaris macandreae.

The bodies of shrimps can offer a substratum for colonization. The ctenostome bryozoan Triticella flava grows a dense 'furry' covering on the antennae, mouthparts and legs of Calocaris macandreae (Hughes, 1998(b)), whilst the mouthparts of Nephrops norvegicus harbour a small commensal sessile animal, the newly described Symbion pandora (Conway Morris, 1995).

Seasonal and longer term change

Amphiura chiajei is a long lived species. Particular cohorts (resultant of a dense and successful larval settlement) may dominate an area for over 10 years and is unlikely to show any significant regular seasonal change in abundance or biomass. However, populations of Amphiura chiajei seem to be periodically affected by winter cold. Mean densities of Amphiura chiajei in Killary Harbour, west coast of Ireland, decreased following months with the lowest recorded bottom temperatures, 4°C and 6°C, for February 1986 and January 1987 respectively. Intolerance of the acute change and depressed temperatures on the part of some older individuals probably led to their demise (Munday & Keegan, 1992).

There are daily patterns of activity in some species. For example, in shallower water, Nephrops norvegicus usually remain within their burrows by day and emerge at dusk to forage during the night. The animals return to their burrows around sunrise. However, in deeper water (> 100 m) this activity rhythm is reversed, and the animals are more active by day.

The distribution of Nephrops norvegicus shows some seasonality. In Loch Sween, Nephrops burrows were aggregated in groups during the late summer, which then broke up into a random distribution during the winter (Tuck et al., 1994). Such aggregations may result when burrow complexes formed when juvenile animals settle in pre-existing adult systems, and later extend their own burrows into other areas.

Habitat structure and complexity

The biotope has very little surface structural complexity as most species are infaunal, however, the bioturbating megafauna can create considerable structural complexity below the surface, relative to sediments that lack such animals. A low-energy hydrodynamic regime is a prerequisite for the existence of the fine sedimentary substrata about which some fauna are highly selective. For instance, Amphiura chiajei occurs in greatest density in habitats with a silt/clay content of 80-90% in association with an organic carbon content of 5-7%, whilst Calocaris macandreae only occurs in areas where silt/clay content is greater than 20%, highest densities occur where silt/clay content greater than 60% (Buchanan, 1963).

Burrows and mounds created by burrowing megafauna may be a conspicuous feature of the sediment surface with arm tips of Amphiura chiajei stretching out over the surface but these are not likely to provide a significant habitat for other fauna. However, the bodies of shrimps can offer a substratum for colonization (see ecological relationships).

Most species living within the sediment are restricted to the area above the anoxic layer, the depth of which will vary depending upon sediment particle size and organic content. Some structural complexity is provided by the burrows of macrofauna. Brissopsis lyrifera maintains a respiratory funnel to the surface, whilst the burrows of Calocaris macandreae and Nephrops norvegicus are more complex. Calocaris macandreae constructs a system of U-shaped tunnels which may reach a depth of 21 cm. Burrows of Nephrops norvegicus may be very large, with tunnels over a metre in length and up to 10 cm in diameter, whilst simple burrows consist of a straight or T-shaped tunnel descending at a shallow angle and penetrating the sediment to a depth of between 20-30 cm. Burrows and the bioturbatory activity that creates them allows a much larger volume of sediment to become oxygenated, enhancing the survival and diversity of a considerable variety of smaller infaunal species (Pearson & Rosenberg, 1978).

Deposit feeders, sort and process sediment particles and may result in destabilization of the sediment, which inhibits survival of suspension feeders. This can result in a change in the vertical distribution of particles in the sediment that may facilitate vertical stratification of some species with particle size preferences. Vertical stratification of species according to sediment particle size has been observed in some soft-sediment habitats (Petersen, 1977).

Productivity

Macroalgae are absent from CMU.BriAchi and consequently productivity is mostly secondary derived from detritus and organic material, although shallower sites may develop an extensive growth of benthic diatoms in the summer (David Hughes, pers. comm.). Allochthonous organic material is derived from anthropogenic activity (e.g. sewerage) and natural sources (e.g. plankton, detritus). Autochthonous organic material is formed by benthic microalgae (microphytobenthos e.g. diatoms and euglenoids) and heterotrophic micro-organism production. Organic material is degraded by micro-organisms and the nutrients recycled. The high surface area of fine particles provides surface for the microflora. Buchanan & Warwick (1974) obtained an estimate of the benthic macrofaunal production in the offshore mud off the Northumberland coast between 1971 - 1972. Eighteen species accounted for 90% of all animals, twelve being polychaetes. Although Calocaris macandreae was the single biomass dominant, polychaetes were responsible for the bulk of the biomass overall. The biomass averaged 3.98 g m², and was slightly lower in winter (3.4 - 3.8 g m²) than summer (4.2 - 4.5 g m²). Larger species with individual weights over 100 mg only occurred sporadically in small numbers, and accounted for 22% of the total biomass. In order of production they were: Ammotrypane aulogaster, Heteromastus filiformis, Spiophanes kroyeri, Glycera rouxi, Calocaris macandreae, Abra nitida, Lumbrineris fragilis and Chaetozone setosa. Their combined annual production was estimated to be 1432 mg m². Of the species characteristic of the CMU.BriAchi biotope, Brissopsis lyrifera and Calocaris macandreae were the only significant producers, 108 mg m² /yr. and 142 mg m² /yr. respectively. The population of Amphiura chiajei in this study had been in decline, between 1961 and 1963 Amphiura chiajei density was 12-15 individuals per m², in 1971 only 2 individuals per m² were recorded. Owing to the species low productivity in this instance the authors discounted Amphiura chiajei from their estimates. However, the arms of Amphiura chiajei are an important food source for demersal fish and Nephrops norvegicus providing significant energy transfer to higher trophic levels. Densities of ca 700 Amphiura chiajei per m² were reported by Keegan & Mercer (1986) in Killary Harbour, Ireland, so the species is likely to be a significant producer in other instances. The estimated total production for the macrofauna was 1738 mg m² per annum.

Recruitment processes

In Brissopsis lyrifera the sexes are separate and fertilization external, with the development of a pelagic larva (Fish & Fish, 1996). The fact that Brissopsis lyrifera is the only heart urchin likely to be found in muddy sediments indicates that the larvae are highly selective, and as Brissopsis lyrifera is a burrower the larval phase is the main dispersive mechanism of the urchin. Echinoderm larvae generally undergo a complicated and protracted metamorphosis. For instance, the larvae of other echinoderms, Echinocardium cordatum and Echinus esculentus remain in the plankton for 40 and 46-60 days respectively (Kashenko, 1994; MacBride, 1914). Thus the larvae of Brissopsis lyrifera probably remain in the plankton for a sufficient length of time to disperse from the location of spawning, or to repopulate an area (Nichols, 1969). However, it is likely that the low-energy hydrodynamic regime of the biotope serves to maintain the benthic population, as larvae are retained and settle back into the parent population. From his observations made off the Northumbrian coast, Buchanan (1967) describes Brissopsis lyrifera as a highly productive, fast growing but short lived species. It becomes sexually mature at around 4 years (test length > 60 mm), spawns in late summer / autumn and dies shortly afterwards. Specimens have not been observed to survive and breed for a second time.

Amphiura chiajei reaches sexual maturity after four years and there is a seasonal cycle in gonad development. Spawning occurs between late summer and middle autumn (Fenaux, 1970). In the laboratory, Fenaux (1970) observed a complete larval metamorphosis to take only 8 days at 18°C. It is not clear whether this is representative of field conditions, at cooler temperatures metamorphosis may take longer, but such an apparently short planktonic existence would limit the species powers of dispersal. Despite spawning annually, successful recruitment tends to be sporadic. A heavy and successful settlement of Amphiura chiajei can dominate an area for over 10 years. The population of Amphiura chiajeithat Buchanan (1964) sampled off the Northumbrian coast showed no evidence of recruitment between 1958 and 1964, despite spawning annually. In such long-lived, adult dominated populations in apparently stable areas, Künitzer (1989) suggested that the survival of recruits was low owing to competition with established adults, which as non-selective surface deposit feeders may take their own newly settled juveniles (0.33 mm disc diameter) as a food item. Where established adult populations have become diminished, successful recruitment has been recorded (Munday & Keegan, 1992).

Female Nephrops norvegicus attain sexual maturity at 2.5-3 years of age at a carapace length of 22 mm (Howard, 1989; Bailey et al., 1986). Males become mature after 3 years at a carapace length of 25 mm. In Scottish waters the eggs are spawned and fertilized between August and November and carried by the females until the larvae hatch between April and August. The larvae spend about 50 days in the plankton before settlement. The juveniles appear to preferentially take up residence in existing adult burrows, constructing their burrows as an extension of these (Tuck et al., 1994).

Calocaris macandreae is a protandrous hermaphrodite (initially male, becoming female in later life) producing eggs between January and February that hatch between September and October. Approximately 100 eggs are produced in each batch and the large larvae have no free-swimming phase before settlement. Individual Calocaris macandreae are very long-lived (9-10 years) and slow growing. It does not mature until five years of age, and only produces two or three batches of eggs in a lifetime. Owing to this life history pattern populations tend to be very stable in number over a 10 year period (Buchanan, 1963; 1974).

Time for community to reach maturity

Limited evidence concerning the community development of this biotope was found. The burrowing megafauna that characterize the biotope vary in their reproductive strategies and longevity. Brissopsis lyrifera is short lived (4 years) but fecund and shows clear evidence of successful and consecutive annual recruitment (Buchanan, 1967). Individuals become sexually mature in their forth year. Amphiura chiajei is longer lived than Brissopsis lyrifera and reaches sexual maturity in its forth year, thus the population structure of these species will not reach maturity for at least this length of time. Once established a cohort of Amphiura chiajei can dominate a population, even inhibiting its own consecutive recruitment, for up to 10 years. Time to reach sexual maturity is longer in Nephrops norvegicus, about 2.5 - 3 years and for the very long-lived Calocaris macandreae individuals off the coast of Northumberland did not become sexually mature until five years of age, and produced only two or three batches of eggs in their lifetime (Buchanan, 1963; 1974). In the biotope, polychaetes account for the vast proportion of the biomass, and these are likely to reproduce annually, be shorter lived and reach maturity much more rapidly. Most of the characterizing species reproduce regularly but recruitment is often sporadic owing to interference competition with established adults of the same and other species.

Owing to the fact that the characterizing species take between 3 and 5 years to reach sexual maturity, it is likely that the time for the overall community to reach a fully diverse state will also be several years. It is likely that the low-energy hydrodynamic regime is an important factor in the maintenance of stable benthic populations in this biotope, as larvae are retained in the vicinity of the parent population.